Integrative Physiological & Behavioral Science

, Volume 39, Issue 4, pp 318–333 | Cite as

Amygdala and periaqueductal gray lesions only partially attenuate unconditional defensive responses in rats exposed to a cat

  • Beatrice M. de Oca
  • Michael S. Fanselow


Defensive responses to a cat were observed in rats given excitotoxic lesions of the central nucleus of the amygdala (ACe), dorsolateral periaqueductal gray (dlPAG), ventral periaqueductal gray (vPAG), or sham lesions. Rats were placed adjacent to a compartment containing a cat. Sham-lesioned rats avoided the area nearest the cat and preferred the area furthest away from the cat. They also exhibited numerous defensive responses including, climbing, escape from the apparatus, and freezing. Rats with lesions of the ACe reacted like the sham lesioned rats by preferring the area of the apparatus furthest from the cat, however they climbed and escaped significantly less than sham lesioned rats. Avoidance of the area adjacent to the cat was attenuated in rats with lesions of the vPAG. Climbing along the walls of the apparatus was also attenuated in rats with lesions of the vPAG. Escapes from the apparatus were not significantly reduced by lesions of the vPAG and dlPAG. Thus, ACe lesions attenuated climbing and eliminated escapes, but did not impair locomotion of the rat away from the cat.


Defensive Behavior Defensive Response Tonic Immobility Ultrasonic Vocalization Central Amygdala 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Adamec, R. (2001). Does long term potentiation in periaqueductal gray (PAG) mediate lasting changes in rodent anxiety-like behavior (ALB) produced by predator stress? Effects of low frequency stimulation (LFS) of PAG on place preference and changes in ALB produced by predator stress.Behavioural Brain Research, 120(2), 111–135.PubMedCrossRefGoogle Scholar
  2. Alheid, G., Do Olmos, J.S., & Beltramino, C.A. (1995). Amygdala and extended amygdala. In Paxinos (Ed.)The rat nervous system (pp. 495–578). New York: Academic.Google Scholar
  3. Amorapanth, P., LeDoux, J.E., & Nader, K. (2000). Different lateral amygdala outputs mediate reactions and actions elicited by a fear-arousing stimulus.Nature Neuroscience, 3(1), 74–79.PubMedCrossRefGoogle Scholar
  4. Bandler, R. & Shipley, M.T. (1994). Columnar organization in the midbrain periaqueductal gray: modules for emotional expression?Trends in Neurosciences, 17(9), 379–389.PubMedCrossRefGoogle Scholar
  5. Bellgowan, P.S.F., & Helmstetter, F.J. (1996). Neural systems for the expression of hypoalgesia during nonassociative fear.Behavioral Neuroscience, 110(4), 727–736.PubMedCrossRefGoogle Scholar
  6. Blanchard, D.C. (1997). Stimulus, environmental, and pharmacological control of defensive behaviors. In M.E. Bouton & M.S. Fanselow (Eds.)Learning, Motivation and Cognition. Washington D.C.: American Psychological Association.Google Scholar
  7. Blanchard, D.C. & Blanchard, R.J. (1972). Innate and conditioned reactions to threat in rats with amygdaloid lesions.Journal of Comparative and Physiological Psychology, 81(2), 281–290.PubMedCrossRefGoogle Scholar
  8. Blanchard, D.C. & Takahashi, S.N. (1988). No change in intermale aggression after amygdala lesions which reduce freezing.Physiology & Behavior, 42(6), 613–616.CrossRefGoogle Scholar
  9. Blanchard, R.J., & Blanchard, D.C. (1971). Defensive reactions in the albino rat.Learning and Motivation, 2, 351–362.CrossRefGoogle Scholar
  10. Blanchard, R.J., & Blanchard, D.C. (1989). Antipredator defensive behaviors in a visible burrow system.Journal of Comparative Psychology, 103, 70–82.PubMedCrossRefGoogle Scholar
  11. Blanchard, R.J., Flannelly, K.J., & Blanchard, D.C. (1986). Defensive behaviors of laboratory and wildRattus norvegicus.Journal of Comparative Psychology, 100(2), 101–107.PubMedCrossRefGoogle Scholar
  12. Bolles, R.C. (1971). Species-specific defense reactions. In F.R. Brush (Ed.),Aversive conditioning and learning. New York: Academic Press.Google Scholar
  13. Bouton, M.E., & Bolles, R.C. (1980). Conditioned fear assessed by freezing and by the suppression of three different baselines.Animal Learning & Behavior, 8, 429–434.CrossRefGoogle Scholar
  14. Campeau, S., & Davis, M. (1995). Involvement of the central nucleus and basolateral complex of the amygdala in fear conditioning measured with fear-potentiated startle in rats trained concurrently with auditory and visual conditioned stimulus.Journal of Neuroscience, 15, 2301–2311.PubMedGoogle Scholar
  15. Choi, J.S., & Brown, T.H. (2003). Central amygdala lesions block ultrasonic vocalization and freezing as conditional but not unconditional responses.Journal of Neuroscience, 23(25), 8713–8721.PubMedGoogle Scholar
  16. Coss, R.G. & Owings, D.H. (1978). Snake-directed behavior by snake naive and experienced California ground squirrels in a simulated burrow.Zeitschrift fuer Tierpsychologie, 48(4), 421–435.Google Scholar
  17. de Oca, B.M., DeCola, J.P., Maren, M.S., & Fanselow, M.S. (1998). Distinct regions of the periaqueductal gray are involved in the acquisition and expression of defensive responses.Journal of Neuroscience, 18(9), 3426–3432.PubMedGoogle Scholar
  18. Diamond, D.M., & Rose, G.M. (1994). Stress impairs LTP and hippocampal-dependent memory.Annals of the New York Academy of Sciences, 746, 411–414.PubMedCrossRefGoogle Scholar
  19. Fanselow, M.S. (1991). The midbrain periaqueductal gray as a coordinator of action in response to fear and anxiety. In A. Depaulis & R. Bandler, (Eds.)The midbrain periaqueductal gray matter: Functional, anatomical, and neurochemical organization. Plenum Press: New York.Google Scholar
  20. Fanselow, M.S. (1994). Neural organization of the defensive behavior system responsible for fear.Psychonomic Bulletin and Review, 1(4), 429–438.CrossRefGoogle Scholar
  21. Fanselow, M.S. (1997). Species-specific defense reactions: Retrospect and Prospect. InLearning, Motivation, and Cognition. M.E. Bouton, & M.S. Fanselow (Eds.). Washington D.C.: American Psychological Association.Google Scholar
  22. Fanselow, M.S. & Lester, L.S. (1988). A functional behavioristic approach to aversively motivated behavior: Predatory imminence as a determinant of the topography of defensive behavior. In R.C. Bolles, & M.D. Beecher (Eds.).Evolution and learning. Hillsdale, NJ: Lawrence Erlbaum Associates.Google Scholar
  23. Fanselow, M.S., Lester, L.S., & Helmstetter, F.J. (1988). Changes in feeding and foraging patterns as an antipredator defensive strategy: A laboratory simulation using aversive stimulation in a closed economy.Journal of the Experimental Analysis of Behavior, 50, 361–374.PubMedCrossRefGoogle Scholar
  24. Fanselow, M.S., Sigmundi, R.A. & Williams, J. (1987). Response selection and the hierarchical organization of species-specific defense reactions: The relationship between freezing, flight, and defensive burying.Psychological Record, 37, 381–386.Google Scholar
  25. Fox, R.J. & Sorensen, C.A. (1994). Bilateral lesions of the amygdala attenuate analgesia induced by diverse environmental challenges.Brain Research, 648(2), 215–221.PubMedCrossRefGoogle Scholar
  26. Griffith, C.R. (1920). The behavior of white rats in the presence of cats.Psychobiology, 2, 19–28.CrossRefGoogle Scholar
  27. Hebert, M.A., Ardid, D., Henrie, J.A., Tamashiro, K., Blanchard, D.C., & Blanchard, R.J. (1999). Amygdala lesions produce analgesia in a novel, ethologically relevant acute pain test.Physiology and Behavior, 67(1), 99–105.PubMedCrossRefGoogle Scholar
  28. Helmstetter, F.J. (1992). The amygdala is essential for the expression of conditional hypoalgesia.Behavioral Neuroscience, 106, 518–528.PubMedCrossRefGoogle Scholar
  29. Helmstetter, F.J. & Fanseow, M.S. (1993). Aversively motivated changes in meal patterns of rats in a closed economy: The effects of shock density.animal Learning & Behavior, 21, 168–175.CrossRefGoogle Scholar
  30. Kalin, N.H., Shelton, S.E., Davidson, R.J., & Kelley, A.E. (2001). The primate amygdala mediates acute fear but not the behavioral and physiological components of anxious temperament.The Journal of Neuroscience, 21(6), 2067–2074.PubMedGoogle Scholar
  31. Killcross, S, Robbins, T.W., & Everitt, B.J. (1997). Different types of fear-conditioned behavior mediated by separate nuclei within amygdala.Nature, 388(24), 377–380.PubMedCrossRefGoogle Scholar
  32. Kim, J.J., Lee, H.J., Han, J.S., & Packard, M.G. (2001). Amygdala is critical for stress-induced modulation of hippocampal long-term potentiation and learning.Journal of Neuroscience, 21(14), 5222–5228.PubMedGoogle Scholar
  33. LeDoux, J.E. (1993). Emotional memory: in search of systems and synapses.Annals of the New York Academy of Sciences, 702, 149–157.PubMedCrossRefGoogle Scholar
  34. LeDoux, J.E., Iwata, J., Cicchetti, P., & Reis, D.J. (1988). Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear.Journal of Neuroscience, 8, 2517–2529.PubMedGoogle Scholar
  35. Lester, L.S. & Fanselow, M.S. (1985). Exposure to a cat produces opioid analgesia in rats.Behavioral Neuroscience, 99, 756–759.PubMedCrossRefGoogle Scholar
  36. Li, C.I., Maglinao, T.L., & Takahashi, L.K. (2004). Medial amygdala modulation of predator odor-induced unconditioned fear in the rat.Behavioral Neuroscience, 118(2), 324–332.PubMedCrossRefGoogle Scholar
  37. Maren, S. (1998). Overtraining does not mitigate contextual fear conditioning produced by neurotoxic lesions of the basolateral amygdala.Journal of Neuroscience, 18(8), 3088–3097.PubMedGoogle Scholar
  38. Maren, S., Aharonov, G., Stote D.L., & Fanselow, M.S. (1996). N-methyl-D-aspartate receptors in the basolateral amygdala are required for both acquisition and expression of conditional fear in rats.Behavioral Neuroscience, 110(6), 1365–1374.PubMedCrossRefGoogle Scholar
  39. McGregor, I.S. & Dielenberg, R.A. (1999). Differential anxiolytic efficacy of a benzodiazepine on first versus second exposure to a predatory odor in rats.Psychopharmacology, 147(2), 174–181.PubMedCrossRefGoogle Scholar
  40. Ramos, C., Leite-Panissi, A., & Menescal-de-Oliveira, L. (2002). Central nucleus of the amygdala and the control of tonic immobility in guinea pigs.Brain Research Bulletin, 58(1), 13–19.CrossRefGoogle Scholar
  41. Roesler, R., Vianna, M.R.M., de-Paris, F., Rodrigues, C., Sant’Anna, M.K., Quevedo, J., & Ferreira, M.B.C. (2000). NMDA receptor antagonism in the basolateral amygdala blocks enhancement of inhibitor avoidance learning in previously trained rats.Behavioural Brain Research, 112(1–2), 99–105.PubMedCrossRefGoogle Scholar
  42. Satinder, K.P. (1976). Reactions of selectively bred strains of rats to a cat.Animal Learning & Behavior, 4 (2), 172–176.CrossRefGoogle Scholar
  43. Selye, H. (1976).Stress in health and disease. Boston: Butterworths.Google Scholar
  44. Silveira, M.C.L., Sandner, G., & Graeff, F.G. (1993). Induction of Fos immunoreactivity in the brain by exposure to the elevated plus maze.Behavioural Brain Research, 56, 115–118.PubMedCrossRefGoogle Scholar
  45. Ulrich, R.E. & Azrin, N.H. (1962). Reflexive fighting in response to aversive stimulation.Journal of the Experimental Analysis of Behavior, 5, 511–520.PubMedCrossRefGoogle Scholar
  46. Walker, D.L. & Davis, M. (1997). Double dissociation between the involvement of the bed nucleus of the stria terminalis and the central nucleus of the amygdala in startle increases produced by conditioned versus unconditioned fear.Journal of Neuroscience, 17(23), 9375–9383.PubMedGoogle Scholar
  47. Walker, D.L., Toufexis, D.J., & Davis, M. (2003). Role of the bed nucleus of the stria terminalis versus the amygdala in fear, stress, and anxiety.European Journal of Pharmacology, 463, 199–216.PubMedCrossRefGoogle Scholar
  48. Wallace, K.J. & Rosen, J.B. (2000). Predator odor as an unconditioned fear stimulus in rats: Elicitation of freezing by trimethylthiazoline, a component of fox feces.Behavioral Neuroscience, 114(5), 912–922.PubMedCrossRefGoogle Scholar
  49. Wiedenmayer, C.P., Goodwin, G.A., & Barr, G.A. (2000). The effect of periaqueductal gray lesions on responses to age-specific threats in infant rats.Developmental Brain Research, 120, 191–198.PubMedCrossRefGoogle Scholar
  50. Zangrossi, H., Jr. & File, S.E. (1994). Habituation and generalization of phobic responses to cat odor.Brain Research Bulletin, 33, 189–194.PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2004

Authors and Affiliations

  1. 1.University of CaliforniaLos Angeles

Personalised recommendations